Citation for this paper:
Limoges, A., Londeix, L., Mertens, K. N., Rochon, A., Pospelova, V., Cuéllar, T. &
Vernal, A. (2018). Identification key for Pliocene and Quaternary Spiniferites taxa
bearing intergonal processes based on observations from estuarine and coastal
environments. Palynology, 42(1), 72-88.
https://doi.org/10.1080/01916122.2018.1465733
UVicSPACE: Research & Learning Repository
_____________________________________________________________
Faculty of Science
Faculty Publications
_____________________________________________________________
Identification key for Pliocene and Quaternary Spiniferites taxa bearing intergonal
processes based on observations from estuarine and coastal environments
Audrey Limoges, Laurent Londeix, Kenneth Neil Mertens, André Rochon, Vera
Pospelova, Tomasa Cuéllar & Anne de Vernal
2018
© 2018
Audrey Limoges, Laurent Londeix, Kenneth Neil Mertens, André Rochon,
Vera Pospelova, Tomasa Cuéllar & Anne de Vernal
. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY-NC-ND) license. http://creativecommons.org/licenses/by/4.0/This article was originally published at:
Full Terms & Conditions of access and use can be found at
https://www.tandfonline.com/action/journalInformation?journalCode=tpal20
Palynology
ISSN: 0191-6122 (Print) 1558-9188 (Online) Journal homepage: https://www.tandfonline.com/loi/tpal20
Identification key for Pliocene and Quaternary
Spiniferites
taxa bearing intergonal processes
based on observations from estuarine and coastal
environments
Audrey Limoges, Laurent Londeix, Kenneth Neil Mertens, André Rochon,
Vera Pospelova, Tomasa Cuéllar & Anne de Vernal
To cite this article: Audrey Limoges, Laurent Londeix, Kenneth Neil Mertens, André Rochon, Vera Pospelova, Tomasa Cuéllar & Anne de Vernal (2018) Identification key for Pliocene and Quaternary
Spiniferites taxa bearing intergonal processes based on observations from estuarine and coastal
environments, Palynology, 42:sup1, 72-88, DOI: 10.1080/01916122.2018.1465733 To link to this article: https://doi.org/10.1080/01916122.2018.1465733
© 2018 The Author(s). Published by AASP –
The Palynological Society Published online: 14 Dec 2018. Submit your article to this journal Article views: 503
View related articles View Crossmark data
Identification key for Pliocene and Quaternary
Spiniferites taxa bearing
intergonal processes based on observations from estuarine and coastal
environments
Audrey Limogesa,b, Laurent Londeixc, Kenneth Neil Mertensd,e, Andre Rochonf, Vera Pospelovag, Tomasa Cuellarh
and Anne de Vernali a
Department of Glaciology and Climate, Geological Survey of Denmark and Greenland (GEUS), Copenhagen, Denmark;bDepartment of Earth Sciences, University of New Brunswick, 2 Bailey Drive, Fredericton, Canada;cUMR 5805 EPOC, CS50023, Allee Geoffroy Saint-Hillaire, Universite de Bordeaux, Pessac Cedex, France;dResearch Unit for Palaeontology Ghent University, Gent, Belgium;eIfremer, LER BO, Station de Biologie Marine, Place de la Croix, Concarneau Cedex, France;fInstitut des sciences de la mer (ISMER), Universite du Quebec a Rimouski, Rimouski, Canada;gSchool of Earth and Ocean Sciences, University of Victoria, Victoria, Canada;hPosgrado en Ciencias del Mar y
Limnologıa, Universidad Nacional Autonoma de Mexico, Coyoacan, Ciudad de Mexico, Mexico;iDepartement des sciences de la Terre et de l’Atmosphere, Geotop, Universite du Quebec a Montreal, Montreal, Canada
ABSTRACT
The use of dinoflagellate cyst assemblages as a tool for palaeo-environmental reconstructions strongly relies on the robustness of cyst identification and existing information on the distribution of the differ-ent species. To this purpose, we propose a functional key for the iddiffer-entification of Pliocene and Quaternary Spiniferites bearing intergonal processes and depict the range of morphological variation of the different species on the basis of new observations from estuarine and coastal regions. Accordingly, the description of Spiniferites mirabilis is emended to include the new subspecies Spiniferites mirabilis subsp. serratus. We also report the occasional presence of intergonal processes in Spiniferites bentorii and Spiniferites belerius. This key aims to facilitate identification of this group of Spiniferites bearing intergonal processes and standardize cyst identification among researchers.
KEYWORDS Dinoflagellate cyst; taxonomy; description; morphological variability; emendations 1. Introduction
All species belonging to the genus Spiniferites are known to always bear processes that are gonal, meaning located at the point of intersection (or triple junction) of three plates (e.g. Williams et al. 1978). However, some Spiniferites species can (consistently or occasionally) bear additional processes that are intergonal, meaning located between these intersections (or triple junctions) (e.g. Evitt1985, p. 71) on so-called sutures that form the boundaries between plates (Evitt 1985, p. 69). Another important morphological feature for such species is the presence of crests or septa, which are raised ridges along the plate boundaries. Some of these crests can be raised close to the distal end of the processes (often located on the antapi-cal side), and in such cases, are antapi-called flanges or wings.
Spiniferites species with intergonal processes are important components of the assemblages from Cretaceous to Quaternary deposits (Figure 1). Their distribution extends from estuarine to open ocean environments, in equatorial to subpolar regions (Zonneveld et al.2013). In modern sediments, Spiniferites mirabi-lis (Rossignol1964) Sarjeant1970and Spiniferites hyperacanthus (Deflandre and Cookson1955) Cookson and Eisenack1974are
the most often recognized species bearing intergonal processes and their cumulative abundances can reach more than 50% of the total dinoflagellate cyst (dinocyst) assemblage in the North Atlantic and adjacent seas (based on the Northern Hemisphere database of modern dinocysts compiled at Geotop (cf. de Vernal et al.2013; seeFigure 2; de Vernal et al.2018)). These are accompanied by Spiniferites bentorii (Rossignol1964) Wall and Dale 1970 and a few other species that will be discussed below.
During routine palynological counts, the assignment of Spiniferites specimens to previously described species is some-times challenged by 1) the emergence of atypical features that are not listed in the original descriptions, such as an apical pro-tuberance, sutural septa, wall surface ornamentation and 2) the presence of intergrading morphological features between dis-tinct taxonomic identities. Deciphering whether a specimen found in sediment is a new form or within a range of acceptable morphological variation can thus be difficult. The decision is generally at the discretion of the analyst and may vary from one person to another. The final diagnostic can further depend upon the study area. As such,“uncommon” features are more common in estuarine environments than in open-ocean regions and palynologists working in estuarine environments might be
CONTACTAudrey Limoges Audrey.Limoges@unb.ca Department of Earth Sciences, University of New Brunswick, 2 Bailey Drive, Fredericton, NB E3B 5A3, Canada.
Supplemental data for this article can be accessedhttps://doi.org/10.1080/01916122.2018.1465733. ß 2018 The Author(s). Published by AASP – The Palynological Society
This is an Open Access article distributed under the terms of the Creative Commons Attribution-NonCommercial-NoDerivatives License (http://creativecommons.org/licenses/by-nc-nd/4.
0/), which permits non-commercial re-use, distribution, and reproduction in any medium, provided the original work is properly cited, and is not altered, transformed, or built upon in
any way.
tempted to refer to an operational species concept rather than to its strict formal description.
The use of a standardized taxonomy through an identifi-cation key with clear criteria is of paramount importance when trying to infer palaeoecological and palaeoceano-graphic information from the dinocyst assemblages. In order to facilitate cyst identification during routine counts, we
present an overview of the Pliocene and Quaternary Spiniferites species described as having intergonal processes and we discuss their range of morphological variation.
2. Methodology
We present new observations of several Spiniferites species bearing intergonal processes extracted from sediment from various estuarine and coastal environments including Alvarado Lagoon (Southwestern Gulf of Mexico), West Lake (Florida, U.S.A.), northeast Pacific Ocean (Gulf of California), Isla San Jose Lagoon (southwest Gulf of California), Gulf of San Jorge (Argentina), Aegean Sea, Marmara Sea, and Mediterranean Sea (Figure 3). The large morphological vari-ability depicted from these regions helps to highlight some parts of the original species descriptions that require further clarification. To ensure a good identification of the morpho-logical features, some terms used in the species descriptions are reviewed inTable 1.
We also provide the current inventory of all Spiniferites species documented from Pliocene and Quaternary sedi-ments that were formally described as consistently or occa-sionally bearing intergonal processes. Their original descriptions are reproduced, in addition to supplementary information based on available literature and our new obser-vations. These descriptions are complemented with sche-matic illustrations and micrograph plates.
2.1. Sample preparations
Microscopy observations were performed on residues extracted from sediments processed using marine palyno-logical analyses following standard laboratory procedures. Samples from the Gulf of Mexico, Gulf of San Jorge and Isla San Jose Lagoon were sieved between 106 and 10mm and digested with warm hydrochloric acid (HCl 10%) and hydro-fluoric acid (HF 40%) at Geotop, UQAM and UQAR (see de Vernal et al.1999). Samples from the northeast Pacific Ocean (Gulf of California) and Aegean Sea were sieved between 120 and 15mm and digested with room-temperature HCl (10%) and HF (40%) in the Paleoenvironmental and Marine Palynology Laboratory at the University of Victoria (cf. Pospelova et al. 2010). The organic residue was mounted onto microscope slides in glycerine gelatin. Light microscope observations were conducted by AL and TC at UQAM (Montreal, Canada), by AR at UQAR (Rimouski, Canada), KNM at Ghent University (Belgium), by LL at University of Bordeaux (France) and by VP at University of Victoria (Canada). For scanning electron micrographs, individual cysts were isolated from sediment samples using a micropipette onto a glass slide, subsequently air-dried and observed by KM using a Hitachi S-3400N (UQAM) and AR using a JEOL JSM-6460LV (UQAR).
3. Observations from estuarine and coastal regions
Coastal and estuarine areas are characterized by stronger and more frequent fluctuations in environmental parameters
S. hainanensis S. bentorii S. asperulus S. nortonensis S. speetonensis S. supparus S. tripus S. hyperacanthus S. mirabilis sensu lato S. twistringiensis S. reductus S.vadnatus S. perforatus S. dentatus S. lenzii CONSISTENT INTERGONALS OCCASIONAL INTERGONALS S. hexatypicus S. strictus HOLOCENE PLEISTOCENE PLIOCENE MIOCENE OLIGOCENE EOCENE PALEOCENE NE O G ENE PA LE OGENE QUATERNARY CRET A CE O US UPPER LOWER S. belerius S. multisphaerus S. spinatus S. ludhanensis S. pacificus
Figure 1. Known biostratigraphical ranges of Spiniferites species bearing inter-gonal processes. Taxa bearing interinter-gonal processes on all the sutures (consist-ent intergonals) are distinguished from those occasionally bearing intergonal processes and rarely on all the sutures (occasional intergonals). Species names written in black are discussed in this contribution, whereas those in grey are not discussed.
compared to the open ocean. As a consequence, cysts recov-ered from such marginal settings are more likely to display a wider range of morphological variability, as a response to fluctuating conditions (cf. Lewis et al. 1999; Ellegaard 2000,
2002; Kouli et al. 2001; Mudie et al. 2001; Pospelova et al.
2004; Mertens et al.2009,2012). In the shallow (2 m depth) Alvarado Lagoon (Figure 3), Spiniferites species with intergo-nal processes are dominant and represent up to 48% of the dinocyst assemblages (see Limoges et al. 2015). However, many of the specimens identified did not match the original
descriptions for Pliocene to Quaternary Spiniferites species with intergonal processes. They show a large range of varia-tions with regards to the number, length and morphology of their processes, as well as the development of septa and the presence or absence of an apical protuberance (see Plates 1–2). Their identification is further complicated by ambigu-ities in the original descriptions or overlap between the descriptions. As a consequence, certain specimens could be attributed to either none or more than one of the formally established species. In spite of the individual features of the
Percentages of total assemblages
< 5 % 5-15 % 15-30 %
30-50 % > 50 %
Figure 2.Modern distribution of Spiniferites mirabilis sensu lato together with Spiniferites hyperacanthus based on the Northern Hemisphere database of modern dinocyst compiled at Geotop (n ¼ 1492; cf. de Vernal et al.2013).
1 2 3 5 78 4 6 9 10
Figure 3.Map showing the locations of the various sites from which specimens are illustrated in plates 1–5: 1. Alvarado Lagoon (Plates 1–2), 2. West Lake (Florida; Plate 4), 3. Northeastern Pacific Ocean (Gulf of California) (Plates 3–4), 4. Isla San Jose Lagoon (Southwest Gulf of California) (Plates 4–5), 5. San Jorge Gulf (Plate 3), 6. Mediterranean Sea (Plate 3), 7. Aegean Sea (Plate 3), 8. Marmara Sea (Plates 3–4), 9. Hainan Island (Plate 4), and 10. Japan (Plate 4).
specimens, the apparently continuous range of morphologies would suggest that it seems rather unlikely that they belong to (a lot of) different species. It points to the need to define unambiguous diagnostic features that a specimen should dis-play for assignation to a given palaeontological species, as well as the importance of including a potential range of mor-phological variations to the descriptions.
Comparison of Spiniferites morphologies from Alvarado Lagoon with those of other estuarine and coastal regions across different latitudes shows that the occurrence of morphotypes is not restricted to this specific subtropical site. For instance, the flange, an important characteristic of Spiniferites mirabilis, fre-quently displays important variations with respect to its height and number of processes included (Plate 3, Figures 1–20). The wall ornamentation of Spiniferites mirabilis is variable, ranging from smooth to microgranular (Plate 3, Figures 10–20). The number of intergonal processes in Spiniferites hyperacanthus and Spiniferites mirabilis varies (Plate 3). Many specimens of Spiniferites mirabilis show a well-developed apical protuberance. Furthermore, Spiniferites specimens from various estuarine regions exhibit fairly high sutural crests (Plate 1,Figures 13–15,
Plate 2,Figures 13–14,Plate 3,Figure 6).
As such, on the basis of our new observations, a number of points could be made regarding the morphological char-acteristics of the taxa:
Spiniferites hyperacanthus and Spiniferites mirabilis exhibit variations with regards to the number of intergonal proc-esses, but always bear at least one intergonal process between gonal processes.
In coastal and estuarine settings, Spiniferites hyperacan-thus sometimes displays reduced processes (<3 mm). The development of an apical boss seems to be an occasional
feature of Spiniferites mirabilis (Plate 2,Figures 4–6and9).
Three to ten processes can be embedded in the flange of Spiniferites mirabilis (Plates 2–3).
Specimens bearing intergonal processes and high sutural crests are relatively common in estuarine environments.
4. Original descriptions of Pliocene and Quaternary Spiniferites species with intergonal processes, comments about occurrence and discussion
We present an overview of Pliocene and Quaternary Spiniferites species described as having intergonal processes. These are reported in alphabetical order. We provide the ori-ginal descriptions of the cysts together with translations, and a discussion. Note that in the section below, Spiniferites nanus Matsuoka 1976 has not been included because it is not possible to unambiguously distinguish its morphology from already described species. We recommend restricting its identification to the holotype. Furthermore, although Spiniferites membranaceus (Rossignol 1964) Sarjeant 1970, Spiniferites lazus Reid 1974 and Rottnestia amphicavata Dobell and Norris in Harland et al. 1980 (now considered a junior synonym of Spiniferites elongatus Reid 1974; see Van Nieuwenhove et al. 2018) have previously been reported to occasionally exhibit intergonal processes (Rochon et al.
1999), new observations could not confirm this to be part of their intraspecific morphological variability. These species are therefore not included here, but are respectively discussed in Gurdebeke et al. (2018) and Van Nieuwenhove et al. (2018).
Division DINOFLAGELLATA (B€utschli1885) Fensome et al.1993, emend. Adl et al.2005
Subdivision DINOKARYOTA Fensome et al.1993
Class DINOPHYCEAE Pascher1914 Table 1. Definitions and illustrations of the morphological terms and concepts used to describe Spiniferites taxa with intergonal processes.
Morphological terminology Definition Illustrations
Gonal processes Processes located at the intersection between three paraplates.
Intergonal processes Processes located on the parasutural boundary between two paraplates.
Morphological concepts Signification
Species with occasional intergonal processes Species that can carry one intergonal process (or two, but no more) along some sutures. Species with consistent intergonal processes Species on which at least one intergonal process
Subclass PERIDINIPHYCIDAE Fensome et al.1993
Order GONYAULACALES Taylor1980
Suborder GONYAULACINEAE (Autonym) Family GONYAULACACEAE Lindemann1928
Subfamily GONYAULACOIDEAE (Autonym) Genus SPINIFERITES Mantell1850emend. Sarjeant1970
Spiniferites asperulus Matsuoka 1983, p. 131–132, Plate 12, Figures 2, 3a–b, 4
Original description (from Matsuoka 1983). The intermedi-ate proximochorintermedi-ate cyst is subspherical to ovoidal in shape,
and consists of two layers, periphragm and endophragm. The endophragm is relatively thick and smooth. The peri-phragm is thin and granular. The gonal processes are conical, and distal ends of secondary furcate branches are bifid. At the proximal base of these processes, parasutural septa become membraneous. Their surface has small grana. This ornamenta-tion is especially well developed in both apical and antapical areas. The parasutural septa are weak but almost complete. The archeopyle is a simple and reduced precingular type made up of loss of the 3’’ paraplate. The paratabulation basically coin-cides with the gonyaulacacean type.
Dimensions. Central body: 48–69 mm in length and 45–64 mm in width. Process length: up to 16 mm (Matsuoka1983).
CONSISTENT INTERGONALS
S. hyperacanthus S. mirabilis subsp. mirabilis
S. bentorii S. ludhamensis S. multisphaerus
S. belerius
Antapical flange
S. mirabilis subsp. serratus
S. hainanensis
No antapical flange
OCCASIONAL INTERGONALS
Invaginaons, bubble-like elements on the wall Scabrate to microgranular wall
S. pacificus Sutural ridges perforated ;
Fenestraons on processes
Processes long, slender and solid ≥ 1 intergonal process along each major suture; Processes long, slender and solid
≥ 3 intergonal processes along each major suture; Processes short and conical
High sutural crests; Processes variable in shape
Low sutural crests; Pear-shaped; Processes variable in shape
Low sutural crests; 2 larger antapical processes
Sutural folds rather than crests; Hollow processes
Processes and wall structure formed by bubble-like elements
(A)
(B)
Figure 4. Schematic representations of the Pliocene and Quaternary Spiniferites species with intergonal processes, divided in two groups of taxa (see alsoTable 2): A) those with consistent intergonals, which include species characterized by intergonal processes on all sutures: Spiniferites hainanensis, Spiniferites hyperacanthus, Spiniferites mirabilis subsp. mirabilis and Spiniferites mirabilis subsp. serratus, and B) those with occasional intergonals, which correspond to the species on which intergonal processes are sometimes present, but rarely on all sutures. This group includes Spiniferites belerius, Spiniferites bentorii, Spiniferites pacificus, Spiniferites ludhamensis and Spiniferites multisphaerus.
Lowest stratigraphic occurrence.Early Miocene (Yun1994)
Comment on occurrence. This species was identified only by a few authors in sediment from the Pacific Ocean (Matsuoka1983; Kurita and Obuse2003).
Discussion.The most distinctive features for this species are the gonal processes with granular and membraneous stalks, and the long secondary branches of the processes. While the diagnosis of this species mentions the presence of occasional
intergonal processes, no intergonal process is visible on the holotype of Spiniferites asperulus. This species is therefore not included in our identification key.
Spiniferites belerius Reid 1974, p. 596–598, Plate 2, Figures 12–13 Plate 4,Figure 16
1
2
3
15
16
14
13
4
9
10
11
12
5
6
7
8
Plate 1. Figures 1–16. Bright field light and SEM micrographs of cysts of Spiniferites with intergonal processes that do not show an antapical flange. All specimens were observed in recent sediment from Alvarado Lagoon. 1–8. Spiniferites hyperacanthus. Low to high focal planes of a specimen with up to three intergonal proc-esses. 9–11. Spiniferites hyperacanthus – short-processed morphotype. Low to high focal views of the same specimen. Note the presence of several short intergonal processes and low sutural crests. 12. Spiniferites hyperacanthus – short-processed morphotype, 13–15. Atypical specimens of Spiniferites hyperacanthus showing high sutural crests. 16. Specimen of Spiniferites hyperacanthus – multi-intergonal morphotype. Specimen displaying fusion between processes and up to four inter-gonal processes. Scale bars¼ 10 mm.
Original description(from Reid1974). Test oval, always wid-est at the girdle; at times constricted towards the poles to give a rounded diamond shape with a clear apical node. The thin smooth surfaced wall is ornamented by gonal trifurcate processes formed from sutural septae [sic]. Septae [sic] form the high antapical “trumpet” shaped process, which charac-terises the species and may also form high membranous flanges. Process tips are trifurcate with recurved bifurcate tips. A relatively narrow 6–8 mm girdle is displaced by one to three times its own width.
Dimensions. Central body: 35–42 mm. Maximum process length 7–10 mm, with posterior process length between 10–15 mm (Reid1974).
Lowest stratigraphic occurrence. late Miocene (Bertini et al.1998).
Comment on occurrence.Since Spiniferites belerius is gener-ally grouped with Spiniferites membranaceus in global data-bases (cf. de Vernal et al. 2013; Zonneveld et al. 2013), it is difficult to assess its individual distribution. However, the list of publications in which Spiniferites belerius is reported (see
1
3
4
6
10
7
8
9
11
12
2
13
5
14
15
16
Plate 2.Figures 1–16. Bright field light and SEM micrographs of cysts of Spiniferites with intergonal processes and characterized by a flange or the development of a relatively high crests on the antapical region. All specimens were observed in recent sediment from Alvarado Lagoon. 1–3. Spiniferites mirabilis. Note the ovoidal shape of the central body and the development of a membrane between some processes, 4. Spiniferites mirabilis with very well developed apical protuberance, 5–11. Different specimens of Spiniferites mirabilis showing well developed flanges. Note that the processes are solid and slender and the sutural crests are very low or absent. 12–16. Specimens showing high sutural crests and the development of a moderately high membrane at the antapical region. Scale bars ¼ 10 mm.
PALYNODATA online database2015) highlights a wide distri-bution ranging from tropical to subpolar environments, from coastal to open-ocean regions.
Discussion.Single specimens of Spiniferites belerius can bear variable process shapes. The wall is smooth and thin. Well-developed sutural membranes are often observed between processes, which are frequently truncated. Intergonal proc-esses are occasionally observed one some sutures.
Spiniferites bentorii (Rossignol 1964, p. 84–85, Plate 1, Figures 3, 3bis. 5–8, Plate 3, Figures 1–3) Wall and Dale 1970, p. 47–48
Plate 4,Figures 14–15
Original description (from Rossignol 1964). Le test est forme
de deux couches, d’epaisseur variable; l’interne participe a la pro-tuberance apicale, et n’est interrompue que par l’archeopyle; l’externe donne naissance aux processus et aux tres legeres cr^etes qui forment les « sutures » ou limites des plaques. L’archeopyle est preforme par une ligne de moindre resistance plus transpar-ente a quelque distance du bord de la 3e plaque precingulaire. Les processus sont en general longs, fins, delies, aux points de jonction de trois plaques. Parfois apparaissent des processus sur-numeraires bifurques au long des sutures meridiennes des grandes plaques pre et post-cingulaires. Certains processus sont particuliers: celui qui occupe le sommet de la protuberance apicale semble seulement bifurque: en realite la troisieme branche est laterale et reduite; le processus situe a la suture de la premiere plaque api-cale, la plaque ventrale et le sommet de la 6e precingulaire trian-gulaire resulte de la coalescence de trois processus, il est large et complexe; enfin, des six processus de la plaque antapicale, les deux dorsaux,a la base de la plaque 3’’’, sont toujours beaucoup plus developpes, plus grands et plus larges que tous les autres; ces grands processus antapicaux sont d’ailleurs un caractere tres constant du genre Hystrichosphaera; ils occupent la m^eme situ-ation que les deux protuberances antapicales de nombreux Dinoflagelles. Les quatre autres processus antapicaux, de taille normale, peuvent ^etre reunis deux par deux du m^eme c^ote par des voilesa leur base, et plus ou moins fusionnes.
Translation(by AL). The cyst is formed by two layers, of vari-able thickness; the internal layer is part of the apical protu-berance, and is only interrupted by the archeopyle; the external layer gives rise to the processes and very slight ridges that form the “sutures” or the plate boundaries. The archeopyle is pre-formed by a more transparent line near the edge of the third precingular plate boundary. The processes are generally long, fine and slender at the junction between three plates. Occasionally, surmounting bifurcate processes appear along the longitudinal sutures of the major pre- and postcingular plates. Some processes are very distinctive: the one located at the top of the apical protuberance appears
only bifurcate: in fact, the third branch is lateral and reduced; the process located on the suture of the first apical plate, the ventral plate and on the top of the triangular sixth pre-cingular plate results from the coalescence of three proc-esses, it is large and complex; finally, of the six processes of the antapical plate, the two dorsal on the basis of plate 3000 are always much more developed, longer and larger than all others; these two large antapical processes represent in fact a very constant feature of Hystrichosphaera; they are located at the same position as the two antapical protuberances of several dinoflagellates. The other four antapical processes, of normal size, can be joined pairwise at the same side by low veils at their basis, and can be more or less fused together.
Dimensions. Central body length: 60–73 mm, width: 45–63 mm. Length of processes: 15–20 mm, 25 mm for the antapical processes (Rossignol1964).
Lowest stratigraphic occurrence. Miocene (Mudie 1989; Manum et al.1989).
Comment on occurrence. In modern sediment, Spiniferites ben-torii has until now only been observed from equatorial to temperate regions, dominantly in coastal environments (Zonneveld et al.2013).
Discussion. Spiniferites bentorii is recognized due to its dis-tinctive pear-shaped central body and a pronounced apical boss. The processes are highly variable in shape and length with the two antapical processes being the longest. In rare cases, the bases of the processes can be fenestrate. The wall surface is smooth to microgranular. Intergonal processes are occasionally present on some sutures.
Comparison. Spiniferites bentorii differs from Spiniferites haina-nensis Sun and Song 1992 by its typical pear-shaped central body and in only carrying occasional intergonal processes. On the contrary, Spiniferites hainanensis bears at least one intergo-nal process on all major sutures. In addition, Spiniferites lazus differs from Spiniferites bentorii by its ovoidal to elongate central body shape and by the occasional presence of intergonal proc-esses on Spiniferites bentorii. Spiniferites bentorii differs from Spiniferites multisphaerus Price and Pospelova2014 only by the absence of bubble-like elements on its wall structure.
Spiniferites hainanensis Sun and Song 1992, p. 49, Plate 1, Figure 12, Plate 2, Figures 1–2
Plate 4,Figures 1–11
Original description(from Sun and Song1992). Body ellips-oidal. Endophragm and periphragm appressed between processes and parasutural ridges. Surface smooth or finely granulated. Processes solid, bases connected by low parasu-tural ridges, which are uniformly perforated at the distal ends. Process tips trifurcate (gonal) or bifurcate (intergonal), primary furcations may be additionally bifurcate. One or two small holes are generally seen in the base or middle part of 3
Plate 3.Figures 1–20. Bright field light and SEM micrographs of cysts of Spiniferites mirabilis from different estuarine and coastal regions. These pictures illustrate the range of variability regarding the number of processes included in the flange, the number of intergonal processes between two adjacent gonal processes, the development of rela-tively high sutural crests between processes on some individuals and the wall ornamentation varying from smooth to microgranular. Note that on all specimens, processes are solid and mostly slender. 1–3. Specimens from the Gulf of California. 4. Specimen from the Aegean Sea. 5–6. Specimens from the Gulf of California. 7. Specimen from the Mediterranean Sea. 8–9. Specimens from the Marmara Sea. 10–20. Specimens from the Gulf of San Jorge. Scale bars ¼ 10 mm.
each process. Paratabulation gonyaulacacean, indicated by processes and parasutural ridges. Archeopyle precingular, operculum free. Paracingulum indicated by parasutural fea-tures. Parasulcus not clear.
Dimensions. Central body length: 42.8–49.0 mm, width 35.0–42.0 mm. Length of processes: 10.5 mm (Sun and Song1992).
Lowest stratigraphic occurrence. Quaternary (Sun and Song1992)
Comment on occurrence. This form has rarely been recog-nized from recent sediment and possibly has been grouped with Spiniferites hyperacanthus or within Spiniferites spp. We nonetheless currently consider that this morphology is not restricted to the region where this species was described
7
6
5
3
2
1
8
9
10
11
12
13
15
16
4
14
Plate 4. Figures 1–16. Bright field light and SEM micrographs of cysts of Spiniferites bearing intergonal processes. 1–6. Spiniferites hainanensis from the Marmara Sea and Black Sea 7–8. Spiniferites hainanensis, from Isla San Jose Lagoon. Note the fenestration on the crests connecting the processes. 9–11. Spiniferites hainanen-sis from location S1, Fangchenggang, Guangxi province (very close to Hainan island). 12–13. Holotype of Spiniferites mirabilis subsp. serratus from the Nishiyama formation, Japan. 14–15. Different views of the same specimen of Spiniferites bentorii showing intergonal processes. Note the typical pear-shaped central body and the well-developed apical protuberance. 16. Spiniferites belerius from Alvarado Lagoon. Scale bars ¼ 10 mm.
(Hainan Island, China) and is, at least, present in other warm environments such as the Gulf of California and Marmara Sea.
Discussion. As observed in specimens from the Marmara Sea, Black Sea and Isla San Jose Lagoon (Southwest Gulf of California), the distinctive features of Spiniferites hainanensis are the fenestrate, moderately elevated crests between the bases of the processes (Plate 4,Figures 1–11). The number of intergonal processes differs from one specimen to another (from one to two between pairs of gonal processes) and even from one suture to another on the same specimen. Development of trabeculae between adjacent process tips also is occasionally observed (seePlate 4,Figure 7).
Comparison. Spiniferites hainanensis is distinguished from Spiniferites hyperacanthus by the presence of uniformly perfo-rated parasutural ridges.
Spiniferites hyperacanthus (Deflandre and Cookson1955, p. 264–265, Plate 6, Figure 7) Cookson and Eisenack1974, p. 59
Plate 1,Figures 1–16
Original description (from Deflandre and Cookson 1955). Shell globular, spherical or almost spherical; polygonal fields characteristic of the genus with fine, sometimes almost indis-tinguishable outlines, the equatorial series recognizable by the alignment of the processes. Stalks of processes long, stiff, often slender, dividing into 3 distinct branches with simple or bifurcate apices, inserted both at the angles of the fields and along their sides, the usual arrangement being 1 process to each angle of the field and 2 along each side.
Dimensions. Central body diameter: 54–59 mm. Length of processes: 13–20 mm (Deflandre and Cookson1955).
Lowest stratigraphic occurrence. Cretaceous (Cookson and Eisenack1974; Manum et al.1989)
Comment on occurrence. Spiniferites mirabilis and Spiniferites hyperacanthus are commonly grouped in global datasets making the assessment of their individual distribu-tion difficult. As a group, they are observed in sediment from tropical to subpolar environments. High occurrences are not-ably found around the Iberian Peninsula, in the Mediterranean Sea and in the Gulf of Mexico (seeFigure 1).
Discussion. Although the morphology of Spiniferites hyper-acanthus shows variations with regard to the length of the processes, these are systematically slender. Specimens usu-ally exhibit two intergonal processes between the gonal processes, but this number can vary from one specimen to another: from one to several intergonal processes. Importantly, the sutural crests are low or absent and are inconspicuous at the antapex (i.e. not higher than anywhere else on the cyst). Morphotypes with short processes (<3 mm) were observed from different estuarine regions (Plate 1,
Figures 9–12). It would be interesting to investigate if the process length variations are driven by environmental fac-tors, as it is the case for some other dinocyst taxa (i.e. changes in salinity and temperature; Wall et al. 1973; Nehring 1994; Dale 1996; Lewis et al. 1999; Ellegaard 2000; Kouli et al. 2001; Mudie et al. 2001; Ellegaard et al. 2002; Mertens et al.2009,2012).
Recommendations.In order to keep potentially useful envir-onmental information, we recommend the use of two infor-mal types during routine counts: specimens with short processes (<3 mm) can be identified as Spiniferites hyperacan-thus – short-process morphotype, and specimens with three or more intergonals between pairs of gonal processes as Spiniferites hyperacanthus– multi-intergonal morphotype.
1
5
6
4
2
3
7
8
Plate 5. Figures 1–8. Bright field light micrographs of cysts of Spiniferites bearing intergonal processes. 1–-3. Spiniferites multisphaerus (photos credit: Andrea Price). 4–6. Spiniferites multisphaerus. 7–8. Different views of the same specimen of Spiniferites ludhamensis from the Israelian coastal plain (Ashdod borehole Reading 167 cm). Scale bars¼ 10 mm.
Spiniferites ludhamensis Head 1996, p. 557, Figure 12, nos. 3–14, Figure 13, Figure 14, nos. 1–3
Plate 5,Figures 6–8
Original description(from Head 1996). Spiniferate cyst with egg-shaped central body. Pedium thin (ca. 0.1mm), appearing as black line in optical section. Luxuria consists of tegillum (< 0.3 mm thick) which, across intratabular areas, has funnel-shaped invaginations whose solid, rod-like bases connect with pedium. Bases generally less than 0.3mm in diameter, mostly spaced about 1.0mm or less apart, appearing as closely spaced dots in surface view. Invaginations absent from parasutural areas, and unsupported tegillum forms par-asutural folds about 1–2 mm high delineating gonyaulacoid paratabulation. Gonal and intergonal processes arise from folds. Processes bifurcate or multifurcate, in some cases with second-order branching, and hollow along their entire length including distal terminal branches. Surface of processes finely and faintly granulate. A tapering, spine-like apical process with smaller side branches, also present. Archeopyle precin-gular, type P(3’’). Operculum monoplacate, free.
Dimensions.Central body diameter: 38 (42.2) 49mm. Length of processes: 10 (12.9) 15mm (Head1996).
Lowest stratigraphic occurrence. Quaternary (ca. 2.4–1.8 Ma) (Head1996)
Comment on occurrence. Originally described from the Gelasian of the Royal Society borehole at Ludham, eastern England (Head 1996), this species was also recognized from upper Quaternary sediment of the Mediterranean Sea (see Mertens et al.2018).
Discussion. The numerous invaginations that characterize the wall structure as well as the thin, hollow processes constitute the most important diagnostic features for this species. This species also exhibits parasutural folds rather than solid crests. The central body is ovoidal and to date, no specimen with an apical protuberance has been observed.
Spiniferites mirabilis (Rossignol 1964, p.86–87, Plate 2, Figures 1–3, Plate 3, Figures 4–5) Sarjeant 1970, p. 76 emend.
Plate 2,Figures 1–16;Plate 3,Figures 1–20
Synonymy. Hystrichosphaera mirabilis Rossignol 1964, p. 86–87, Plate 2, Figures 1–3, Plate 3, Figures 4–5 (the species was first invalidly published by Rossignol 1962, p. 132, because no image was provided); Spiniferites mirabilis (Rossignol) Sarjeant 1970, p. 76; Spiniferites splendidus Harland1979, p. 537, Plate 3, Figures 1–2.
Original description(from Rossignol1964). La paroi est fine, a deux couches. Les «sutures» des plaques sont peu discern-ables a cause du grand nombre de processus qui s’y dressent. Au p^ole antapical, la ou chez Hystrichosphaera furcata s’elevent les deux grands processus dorsaux, la serie des 5 a 7 processus inseres sur la face dorsale et les faces laterales de la plaque antapicale est noyee dans un voile commun qui les
emp^ate jusqu’a la fourche; il est constitue comme les processus eux-m^emes, par la couche externe du test, decollee de la couche interne; vus de face, ces processus forment une sorte d’eventail; vu de profil, leur base commune prend l’aspect de doigts de gant les uns derriere les autres; en vue antapicale, cet eventail forme un fer a cheval ouvert sur la face ventrale de l’hystrichosphere.
Translation (by AL). The wall is thin and consists of two layers. The plate “sutures” are weakly discernible due to the presence of the large number of processes that they carry. At the antapical pole, where two large dorsal processes rise on Hystrichosphaera furcata, a series of five to seven proc-esses located on the dorsal and lateral sides of the antapical plates are embedded in a shared veil, which rises to the dis-tal end of the processes; just like the processes, the veil forms from the external layer of the cyst, detached from the internal layer; in frontal view, these processes appear like a hand fan; in lateral view, their joined basis looks like the fin-gers of a glove, one behind the other; in antapical view, this fan takes on the appearance of a horseshoe that opens to the ventral side of the hystrichosphere.
Emended diagnosis. Ovoidal to spheroidal cyst character-ized by a noticeable flange between dorsal antapical proc-esses. Processes are both gonal (trifurcate) and intergonal (bifurcate) with recurved bifurcate tips– at least one intergo-nal process is present on all sutures. The wall surface orna-mentation ranges from smooth to granulate. Sutural crests are absent to moderately high. The archeopyle is precingular and formed by loss of plate 3’’.
Emended description. Central body ovoidal to spheroidal. The wall is thin and consists of two layers. The wall surface ornamentation ranges from smooth to granulate. Sutural crests are generally low, and can be nearly absent. However, the emergence of moderately high sutural crests between processes can be observed on certain specimens (see Plate 3,Figure 6). Gonal processes are trifurcate with bifurcate tips. Intergonal processes are bifurcate with bifurcate tips. Although Spiniferites mirabilis exhibits significant variations with regards to the number of intergonal processes (from one to more than three) (Plates 2–3and specimen illustrated in Rochon et al.1999), at least one intergonal process is pre-sent on all sutures. A flange, composed of a variable number of processes, is present on the dorsal side of the antapical plate. The number and length of the processes included in the flange varies from one specimen to another and up to 10 processes were counted on specimens illustrated here (seePlates 2 and3). The antapical flange can be asymmetric (e.g. Mao and Harland 1993, Plate 1, Figure 3; Morzadec-Kerfourn2002, Plate 1, Figure 3; Limoges et al.2013, Plate 2, Figure 17) and is located along the suture separating plates 4’’’ and 1’’’’. The paratabulation formula is 4’, 6’’, 6c, xs, 6’’’, 1p, 1’’’’
Dimensions. Central body diameter: 40–84 mm in length, 35–76 mm in width. Length of processes: 7–44 mm.
Lowest stratigraphic occurrence. Late Cretaceous (Kedves1999).
Discussion about subdivision of the species. The descrip-tion of Spiniferites mirabilis is here emended to include its
range of morphological variability. There is no clear bio-logical evidence to know whether the number of intergonal processes has any importance to differentiate species (inter-specific variation), subspecies (intra(inter-specific variation) or can vary within a single strain. This missing evidence results in inconsistency in the current descriptions of species. Some species have been differentiated based on their number of intergonal processes, notably to differentiate Spiniferites ser-ratus Matsuoka 1983 from Spiniferites mirabilis, whilst other species such as Spiniferites hyperacanthus have been allowed variation of the number of intergonal processes. Given the missing biological evidence, in this paper we chose to try to retain as much as possible information. Hence, considering the large range of morphological variability associated to Spiniferites mirabilis, we here propose to retain two subspecies: Spiniferites mirabilis subsp. serratus new subspecies, and Spiniferites mirabilis subsp. mirabilis (autonym). This subdivision is based on the number of intergonal processes between pairs of gonal proc-esses and on the general shape of the procproc-esses. Spiniferites mirabilis subsp. mirabilis exhibits at least one intergonal process between adjacent gonal processes, whereas Spiniferites mirabilis subsp. serratus exhibits at least three intergonal processes between gonal processes. The processes of Spiniferites mirabilis subsp. serratus are shorter and flatter than those of Spiniferites mirabilis subsp. mirabilis.
Note. The holotype could not be localized; it is therefore impossible at this moment to comment on it.
Comparison.The main feature to distinguish Spiniferites mir-abilis from Spiniferites hyperacanthus is the presence of a well-developed flange along the suture between the antapi-cal (1’’’’) and 3’’’ plates. This feature is absent on Spiniferites hyperacanthus.
Spiniferites mirabilis subsp. mirabilis (autonym) (Rossignol 1964, p. 86–87, Plate 2, Figures 1–3, Plate 3, Figures 4–5) Sarjeant1970, p. 76 emend.
Diagnosis. A subspecies of Spiniferites mirabilis on which one or two intergonal processes are present between two adjacent gonal processes. Processes are generally long and slender.
Dimensions. Central body diameter: 40–70 mm in length, 35–60 mm in width. Length of processes: 15–22 mm (Rossignol1964).
Discussion. Spiniferites mirabilis subsp. mirabilis differs from Spiniferites mirabilis subsp. serratus in having less than three intergonal processes between pairs of gonal processes. Spiniferites mirabilis subsp. serratus (Matsuoka 1983)
stat. nov.¼ Spiniferites serratus Matsuoka 1983, p. 135–136, Plate 14, Figures 1a–c, 2a–c, 3
Plate 4,Figures 12–13
Synonymy. Spiniferites serratus Matsuoka 1983, p. 135–136, Plate 14, Figures 1a–c, 2a–c, 3, Figure 20, A–B (pro-posed here).
Diagnosis.A subspecies of Spiniferites mirabilis, which exhib-its three or more intergonal processes between two adjacent
gonal processes, and relatively shorter and flatter processes than that of Spiniferites mirabilis subsp. mirabilis.
Description. Central body ovoidal to spheroidal. The wall is thin and consists of two layers. Sutural crests are generally low, except at the antapex, where they form a flange. Processes are conical to subconical. Three or more intergonal processes are present on all major sutures. The archeopyle is a reduced pentagonal and simple precingular type derived from loss of the 3” paraplate.
Dimensions. Central body diameter: 45–54 mm in body length, 47–50 mm in body width. Length of processes: 7–9 mm (Matsuoka1983).
Lowest stratigraphic occurrence. late Neogene (Matsuoka
1983; Bujak and Matsuoka1986)
Comment on occurrence. A few authors have reported this form in samples from the Pacific Ocean (Yun et al. 1999,
2000; Kurita and Obuse2003).
Discussion. Most of the morphologic features (archeopyle, flange, central body shape) of Spiniferites serratus conform to those of Spiniferites mirabilis. However, Spiniferites serratus was described by Matsuoka (1983) as a species distinct from Spiniferites mirabilis on the basis of its relatively smaller size and the presence of at least three intergonal processes between each gonal process. Here, we propose the following change in rank: Spiniferites mirabilis subsp. serratus (Matsuoka
1983) stat. nov.¼ Spiniferites serratus Matsuoka 1983, p. 135–136, Plate 14, Figures 1a–c, 2a–c, 3.
Spiniferites multisphaerus Price and Pospelova 2014, p. 101–116, Plate 1–2, Plate 3, Figures 7–9, Plate 4, Figures 4–11, Plate 5, Figures 4–9
Plate 5,Figures 1–5
Original description (from Price and Pospelova 2014). Oval to pear-shaped, proximochorate cyst with a pronounced apical protuberance. Wall is relatively thick and is con-structed of small bubble-like elements. Processes are stubby, furcate and contain hollow bubble-like elements. Tabulation is clearly expressed and is typical of the genus. Archeopyle precingular, formed by release of Plate 3’’.
Dimensions. Range central body length (including apical protuberance): 42.6 (52.4) 66.5mm. Mean length of processes: 1.5 (4.4) 8.0mm (Price and Pospelova2014).
Lowest stratigraphic occurrence. Late Pleistocene (Price and Pospelova2014)
Comment on occurrence. To date, this species has only been documented from the central to northern Gulf of California, where it was described.
Discussion. This species differs from the others by the wall structure, sutural septa and processes that feature bubble-like elements (Plate 5,Figures 1–5). The wall surface is pitted or reticulate. We refer to the round table discussion (Mertens et al. 2018) for comparison with other Spiniferites species that have a bubble-like surface texture.
Spiniferites pacificus Zhao and Morzadec-Kerfourn 1994, p. 268–269, Plate 1, Figures 1 a–c, 2 a–b, 3, Plate 2, Figures 1–2–3 a–b
Original description (from Zhao and Morzadec-Kerfourn
1994). Kyste proximochorate de forme spherique a ovoïde dont la paroi est composee d’un endophragme et d’un periphragme a surface microgranuleuse. Presence de proc-essus gonauxa extremite trifurquee puis bifurquee, de proc-essus intergonaux a extremite bifurquee et de deux processus antapicaux, creux, plus developpes que les autres, relies par une membrane septale basse et ouverts a leur extremite divisee en trois longues branches a terminai-son bifurquee.
Translation (by AL). Proximochorate cyst, subspherical to ovoidal in shape, having a wall that consists of an endro-phragm and a periendro-phragm with a microgranular surface. Presence of gonal processes with trifurcate terminations and birfurcate tips, intergonal processes with bifurcate ter-minations, and two hollow antapical processes, that are more developed than the others, linked together by a low septal membrane and open at their extremity, which is divided in three long branches with bifurcated terminations.
Dimensions.Central body diameter: 30–35 mm. Mean length of processes: 10mm. Mean length of antapical processes: 13mm (Zhao and Morzadec-Kerfourn1994).
Lowest stratigraphic occurrence. Pleistocene (Zhao and Morzadec-Kerfourn1994)
Comment on occurrence. This species was described from the northwest Pacific Ocean.
Discussion. In the original description, Spiniferites pacificus differs from the other Spiniferites species in having stout and distally open antapical processes. Processes are sometimes connected by low crests.
Spiniferites spinatus (Song et al. 1985, p. 43, Plate 2, Figure 5) Lentin and Williams1989
Translation(by Haifeng Gu, Third Institute of Oceanography, Xiamen – China, February 2017). Cyst ovoid to subspherical, epicyst and hypocyst equal in size separated by a wide and clear cingulum. The cyst wall probably consists of two rela-tively thin layers, whose surface is coarse to granular. The archeopyle is difficult to be identified. The cyst is a typical spiniferate, with large and marked plates of epicyst and hypocyst, and cingular plates extending in horizontal direc-tion. The paraplates are demarcated by subtle ridges 2–3 mm high, like one layer of thin membrane surrounding the cyst body. There are short tubular processes at the junctions of ridges, which are narrow, hollow with trifurcate or bifurcate distal ends. There are ca. 2 spiny processes in the middle of the ridges whose bases are wide and taper abruptly with pointed distal end. The ridges are smooth. The diameter of the cyst body is 38mm and the processes can be as high as 5mm. The current specimen has a plate pattern identical to Spiniferites cingulatus Sarjeant 1970 (Eisenack, Katalog, Bd. II, pp. 537). Spiniferites cingulatus comprises several varieties based on the ornamentations of cyst body and overall cyst shape, which all possess high ridges and clear plate bounda-ries. The current variety has weak ridges and spiny processes
in the ridges, which can be differentiated from previ-ous varieties.
Dimensions. Central body: 47–60 x 35–56 mm. Length of processes: 5mm (Song et al.1985).
Lowest stratigraphic occurrence. Early Pleistocene (Lentin and Williams,1989)
Comment on occurrence. To date, this taxon was observed exclusively in the type material of the Pacific Ocean, East China Sea.
Recommendation. We recommend restricting the identifica-tion of Spiniferites spinatus to the holotype. This species is therefore not included in the identification key.
Spiniferites splendidus Harland 1979, p. 537, Plate 3, Figures 1–2. ¼ Spiniferites mirabilis emend.
Original description(from Harland1979). Some specimens of this species are broader than long and exhibit some separation of the wall layers beneath the processes giving rise to bulbous process bases. The cyst is characterized, however, by its large size and by the distinctive morph-ology of the processes. The membranous processes are particularly conspicuous especially those in the posterior intercalary position. The tabulation is outlined by low ridges or membranes, which are confluent with the pro-cess structure.
Dimensions. Central body: 62.0–84.0 mm in length, 52.0–76.0 mm in width. Length of processes: 22.0–44.0 mm (Harland1979).
Lowest stratigraphic occurrence. Senonian, Cretaceous (Kedves1999)
Comment on occurrence. Spiniferites splendidus has been mainly identified from Neogene sediment in the North Atlantic region (e.g. McCarthy and Mudie1996).
Discussion. Spiniferites splendidus was described by Harland (1979) as a separate species from Spiniferites mirabilis on the basis of its larger size and the presence of numerous flam-boyant membranous processes. After examination of new photographs of the holotype of Spiniferites splendidus and given the large intraspecific variability within Spiniferites mir-abilis, Spiniferites splendidus is now considered to be a junior synonym of Spiniferites mirabilis.
Spiniferites strictus Matsuoka1983, p. 136–137, Plate 12, Figures 4a–b, 6
Original description (from Matsuoka 1983). The intermedi-ate proximochorintermedi-ate cyst is subspherical to ovoidal in shape, and consists of two layers, moderately thick periphragm with a smooth to granular surface and endophragm, adpressed between processes. The processes comprise relatively short tapering gonal and intergonal types. They have bi- or trifur-cate second branches with bifid tips. Small perforations are sometimes observed near the proximal base of the proc-esses. The parasutural septa are distinctive and somewhat membraneous. Some specimens have a small apical boss, but not always. The archeopyle is a reduced pentagonal
precingular type derived from release of the 3’’ paraplate. The paratabulation is that of the genus.
Dimensions. Central body: 53–67 in length, 50–62 mm in width. Length of processes: 10–14 mm (Matsuoka1983).
Lowest stratigraphic occurrence. Miocene (Suzuki and Kurita1998)
Comment on occurrence. This species was rarely reported from the Pacific and Atlantic Oceans (Matsuoka 1983; Engel
1992; Yun et al.2000).
Discussion. It is difficult to unambiguously differentiate this morphology from that of Spiniferites bentorii. We therefore suggest restricting the name to the holotype. This species is not included in the identification key.
6. Identification key for Spiniferites taxa with intergonal processes
On the basis of our observations and the available literature, we propose to separate the Spiniferites taxa with intergonal processes into two morphological groups (Table 2,Figure 4): 1. Those bearing consistent intergonal processes, which
include species characterized by at least one intergonal process on all sutures. For Pliocene and Quaternary strata, this group includes Spiniferites hainanensis, Spiniferites hyperacanthus, Spiniferites mirabilis subsp. mir-abilis and Spiniferites mirmir-abilis subsp. serratus stat. nov. 2. Those bearing occasional intergonal processes, which
cor-respond to the species on which such processes are some-times present, but rarely on all sutures. This group includes Spiniferites belerius, Spiniferites bentorii as the most common species, in addition to Spiniferites ludhamensis, Spiniferites multisphaerus and Spiniferites pacificus.
Beyond the distribution of intergonal processes, consistent or occasional, a number of criteria have to be taken into account. The shape and number of intergonal processes, the height of the sutural crests and the presence or absence of a flange are the most important features for assigning a
specimen to a given species. We do not consider the pres-ence or abspres-ence of an apical boss to be a significant mor-phological trait to separate species or even subspecies. For instance, we demonstrated that such feature is recurrent for Spiniferites mirabilis. Indeed, cysts formed in batch cul-tures of single strains have also shown the presence and absence of an apical boss (e.g. Lewis et al.2001).
7. Conclusion
The list of eight species of Spiniferites bearing intergonal processes observed from Pliocene and Quaternary sediments is provided. Although some morphological variations can be accepted and should not compromise routine cyst identifica-tion, especially when working in estuarine environments, we highly recommend illustrating forms that show atypical fea-tures to allow for site-to-site comparison of the different morphotypes. This might help to extract a potential environ-mental significance for the emergence of certain structures.
A few suggestions were made according to our observations:
We recommend the originally defined Spiniferites serratus to be regarded as a morphological variability of Spiniferites mirabilis, i.e. Spiniferites mirabilis subsp. serratus.
We propose Spiniferites splendidus to be regarded as a junior synonym of Spiniferites mirabilis.
We suggest the occasional presence of intergonal proc-esses to be part of the intraspecific variability of Spiniferites bentorii and Spiniferites belerius.
We informally suggest identifying specimens of Spiniferites hyperacanthus with three or more intergonal processes between pairs of gonal processes as Spiniferites hyperacanthus – multi-intergonal morphotype. Similarly, we suggest identifying specimens of Spiniferites hyper-acanthus with short processes (<3 mm) as Spiniferites hyperacanthus– short-process morphotype.
Table 2. Identification key for Pliocene and Quaternary Spiniferites taxa bearing intergonal processes (see alsoFigure 4). Consistent
intergonals
One or more intergonal processes along each majora parasu-tural boundaries
No antapical flange Sutural ridges uniformly perforated at the base of the processes
Spiniferites hainanensis Long processes (R>0.20) Spiniferites hyperacanthus Short processes (R<0.06) Spiniferites hyperacanthus –
short-process morphotype Antapical flange At least 1 intergonal along each major
bound-ary; Processes long, slender and solid
Spiniferites mirabilis subsp. mirabilis
At least 3 intergonals along each major bound-ary; Short, conical processes
Spiniferites mirabilis subsp. serratus
Occasional intergonals
Occasional intergonal processes (not more than one or two) along some meridian parastu-tural boundaries
Wall bi-layered with scabrate to microgranular periphragm
High sutural crests; Processes variable in shape within a same specimen and
fre-quently truncated
Spiniferites belerius Low sutural crests; Pear-shaped central body Spiniferites bentorii Processes connected by low crests; Two larger
and thicker processes near the antapex
Spiniferites pacificus Wall bi-layered with
invaginations or buble-like elements
Sutural folds rather than solid crests; Processes are hollow along their entire length and arise from folds
Spiniferites ludhamensis Pitted surface to micro-vesicular periphragm;
Processes and wall structure formed by mul-tiple bubble-like elements
Spiniferites multisphaerus a
Meridian pre- and post-cingular plate boundaries. R ¼ length of processes/diameter of the central body.
Acknowledgments
We thank Kazumi Matsuoka for kindly accepting that we re-photograph the holotype of Spiniferites serratus and use these images in the present contribution. We also thank Rex Harland and James Riding for providing the re-photographs of the holotype of Spiniferites splendidus. We also thank Andrea M. Price for providing new pictures of Spiniferites multi-sphaerus and Haifeng Gu for having kindly translated the description of Spiniferites spinatus. Special thanks go to Stijn De Schepper and Frederique Eynaud for their very constructive and helpful reviews of the manuscript.
Funding
Financial support to AL and AdV from the Fonds de Recherche du Quebec - Nature et Technologies (FRQNT) and to AdV, VP and AR from Natural Sciences and Engineering Research Council (NSERC) of Canada are gratefully acknowledged.
References
Adl SM, Simpson AGB, Farmer MA, Andersen RA, Anderson OR, Barta JR, Bowser SS, Brugerolle G, Fensome RA, Fredericq S. 2005. The new higher level classification of Eukaryotes with emphasis on the tax-onomy of Protists. J Eukaryot Microbiol. 52(5):399–451.
B€utschli O. 1885. Erster Band. Protozoa. 3. Unterabtheilung (Ordnung) Dinoflagellata. In: Dr. H.G. Bronn’s Klassen und Ordnungen des Thier-Reichs, wissenschaftlich dargestellt in Wort und Bild. C.F. Leipzig and Heidelberg: Winter’sche Verlagshandlung; p. 906–1029.
Bertini A, Londeix L, Maniscalco R, Stefano AD, Suc J-P, Clauzon G, Gautier F, Grasso M, Gautier F.1998. Paleobiological evidence of dep-ositional conditions in the Salt Member, Gessoso-Solfifera Formation (Messinian, Upper Miocene) of Sicily. Micropaleontology. 44(4):413–433.
Bujak JP, Matsuoka K.1986. Late Cenozoic dinoflagellate cyst-zonation in the Western and northern Pacific. AASP Contribution Series. 17:7–25. Cookson IC, Eisenack A.1974. Mikroplankton aus australischen
mesozoi-schen und terti€aren Sedimenten. Palaeontogr Abt B. 148:44–93. Dale B. 1996. Dinoflagellate cyst ecology: modelling and geological
applications. In: Jansonius J, McGregor DC, editors. Palynology: princi-ples and applications. Vol. 3. Dallas, TX: AASP Foundation; p. 1249–1275.
Deflandre G, Cookson IC.1955. Fossil microplankton from Australian Late Mesozoic and Tertiary sediments. Aust J Mar Freshwater Res. 6(2):242–313.
de Vernal A, Henry M, Bilodeau G.1999. Techniques de preparation et d’analyse en micropaleontologie. Les Cahiers Du GEOTOP. 1–28. de Vernal A, Eynaud F, Henry M, Limoges A, Londeix L, Matthiessen M,
Marret F, Pospelova V, Radi T, Rochon A, et al.2018. Distribution and (paleo)ecological affinities of the main Spiniferites Taxa in the Mid-High Latitudes of the Northern Hemisphere. Palynology. 42(S1). doi:10.1080/01916122.2018.1465730
de Vernal A, Rochon A, Frechette B, Henry M, Radi T, Solignac S.2013. Reconstructing past sea ice cover of the Northern Hemisphere from dinocyst assemblages: status of the approach. Quaternary Sci Rev. 79:122–134.
Ellegaard M. 2000. Variations in dinoflagellate cyst morphology under conditions of changing salinity during the last 2000 years in the Limfjord, Denmark. Rev Palaeobot Palynol. 109(1):65–81.
Ellegaard M, Lewis J, Harding I. 2002. Gonyaulax baltica sp. nov. (Dinophyceae) - cyst-theca relationship, life cycle and environmentally induced morphological variations in the cyst of a new species from the Baltic. J Phycol. 38(4):775–789.
Engel ER. 1992. Palynological evidence of climatically relevant events from Miocene sediments from the North Atlantic. Geologisches Jahrbuch Reihe A. 125:3–139.
Evitt WR.1985. Sporopollenin dinoflagellate cysts: their morphology and interpretation. American Association of Stratigraphic Palynologists. Monogr Ser. 1:333.
Fensome RA, Taylor FJR, Norris G, Sarjeant WAS, Wharton DI, Williams GL. 1993. A classification of fossil and living dinoflagellates. Micropaleontol Special Publ. 7:1–245.
Gurdebeke PR, Mertens KN, Bogus K, Marret F, Chomerat N, Vrielinck H, Louwye S.2018. Taxonomic re-investigation and geochemical charac-terization of Reid’s 1974 species of Spiniferites from holotype and top-otype material. Palynology. 42(S1). doi:10.1080/ 01916122.2018.1465735
Harland R. 1979. Dinoflagellate biostratigraphy of Neogene and Quaternary sediments at holes 400/400A in the Bay of Biscay (Deep Sea Drilling Project Leg 48). In: Montadert, L. et al., editors. Deep Sea Drilling Project, Washington, Initial Reports 48, p. 531–545.
Head MJ. 1996. Late Cenozoic dinoflagellates from the Royal Society borehole at Ludham, Norfolk, eastern England. J Paleontol. 70(04):543–570.
Kedves M. 1999. Organic microfossils from Hungarian Cretaceous sedi-ments. Plant Cell Bio Develop. 11:19–33.
Kouli K, Brinkhuis H, Dale B. 2001. Spiniferites cruciformis: a fresh water dinoflagellate cyst? Rev Palaeobot Palynol. 113(4):273–286.
Kurita H, Obuse A. 2003. Middle Miocene–uppermost lower Pliocene dinoflagellate cyst biostratigraphy, ODP Leg 186 Hole 1151A, off Sanriku Coast of northern Japan, northwestern Pacific. In: Suyehiro K, Sacks IS, Acton GD, Oda M., editors. College Station, TX: Ocean Drilling Program, proceedings, scientific results, Leg 186; p. 1–19. Lentin JK, Williams GL.1989. Fossil dinoflagellates: index to genera and
species, 1989 edition. Dallas, TX: American Association of Stratigraphy Palynologists Foundation, AASP Contribution Series 20, 473 pp. Lewis J, Rochon A, Harding I. 1999. Preliminary observations of
cyst-theca relationships in Spiniferites ramosus and Spiniferites membrana-ceus (Dinophyceae). Sgra. 38(2):113–124.
Lewis J, Rochon A, Ellegaard M, Mudie PJ, Harding I.2001. The cyst-theca relationship of Bitectatodinium tepikiense (Dinophyceae). Euro J Phycol. 36(2):137–146.
Limoges A, Londeix L, de Vernal A.2013. Organic-walled dinoflagellate cyst distribution in the Gulf of Mexico. Mar Micropaleontol. 102:51–68.
Limoges A, de Vernal A, Ruiz-Fernandez A-C. 2015. Investigating the impact of land use and the potential for harmful algal blooms in a tropical lagoon of the Gulf of Mexico. Estuar Coast Shelf S. 167:549–559.
Lindemann E.1928. Abteilung Peridineae (Dinoflagellatae). In: Engler A, Prantl K, editors. Die Nat€urlichen Pflanzenfamilien nebst ihren Gattungen und wichtigeren Arten insbesondere den Nutzpflanzen. Zweite stark vermehrte und verbesserte Auflage herausgegeben von A. Engler. 2 Band. Leipzig: Wilhelm Engelmann; p. 3–104.
Mantell GA. 1850. A pictorial atlas of fossil remains consisting of col-oured illustrations selected from Parkinson’s “Organic Remains of a Former World”, and Artis’s “Antediluvian Phytology”. London (UK): Henry G. Bohn.
Manum SB, Boulter MC, Gunnarsdottir H, Rangnes K, Scholze A. 1989. Eocene to Miocene palynology of the Norwegian Sea (ODP Leg 104). In: Eldholm O, Thiede J, Taylor E, editors. College Station, TX: Ocean Drilling Program, Proceedings, Scientific Results, Leg. 105, p. 611–662. Mao S, Harland R. 1993. Quaternary organic-walled dinoflagellate cysts from the South China Sea and their paleoclimatic significance. Palynology. 17(1):47–65.
Matsuoka K. 1983. Late Cenozoic dinoflagellates and acritarchs in the Niigata district, central Japan. Palaeontogr Abt B. 187:89–154. McCarthy FMG, Mudie PJ.1996. Palynology and dinoflagellate
biostratig-raphy of Upper Cenozoic sediments from Sites 898 and 900, Iberia Abyssal Plain. In: Whitmarsh RB, Sawyer DS, Klaus A, Masson DG, edi-tors. College Station, TX: Ocean Drilling Program, Proceedings, Scientific Results, Leg. 149; 241–265.
Mertens KN, Ribeiro S, Bouimetarhan I, Hulya C, Nebout NC, Dale B, de Vernal A, Ellegaard M, Filipova M, Godhe A, et al.2009. Process length variation in cysts of a dinoflagellate, Lingulodinium machaerophorum,
in surface sediments: investigating its potential as salinity proxy. Mar Micropaleontol. 70(1–2):54–69.
Mertens KN, Bradley LR, Takano Y, Mudie PJ, Marret F, Aksu AE, Hiscott RN, Verleye TJ, Mousing EA, Smyrnova LL, et al. 2012. Quantitative estimation of Holocene surface salinity variation in the Black Sea using dinoflagellate cyst process length. Quaternary Sci Rev. 39:45–59. Mertens KN, Van Nieuwenhove N, Gurdebeke PR, Aydin H, Bogus K, Bringue M, Dale B, De Schepper S, de Vernal A, Ellegaard M, et al. 2018. Summary of round table discussions about Spiniferites and Achomosphaera occuring in Pliocene to modern sediments. Palynology. 42(S1). doi:10.1080/01916122.2018.1465739
Morzadec-Kerfourn MT.2002. L’evolution des Sebkhas du golf de Gabes (Tunisie) a la transition Pleistocene superieur-Holocene. Quaternaire. 13:111–123.
Mudie PJ, et al. 1989. Palynology and dinocyst biostratigraphy of the late Miocene to Pleistocene, Norwegian Sea: ODP Leg 104, Sites 642 to 644. In: Eldholm O, Thiede J, Taylor E, editors. College Station, TX: Ocean Drilling Program, Proceedings, Scientific Results, Leg. 104; p. 587–610.
Mudie PJ, Aksu AE, Yasar D.2001. Late Quaternary dinoflagellate cysts from the Black, Marmara and Aegean seas: variations in assemblages, morphology and paleosalinity. Mar Micropaleontol. 43(1–2):155–178. Nehring S. 1994. Spatial distribution of dinoflagellate resting cysts in
recent sediments of Kiel Bight, Germany (Baltic Sea). Ophelia. 39(2):137–158.
PALYNODATA online database [internet] 2015. Available from: http:// paleobotany.ru/(consulted December).
Pascher A. 1914. €Uber Flagellaten und Algen. Berichte Der Deutschen Botanischen Gesellschaft. 32:136–160.
Pospelova V, Chmura GL, Walker HA.2004. Environmental factors influ-encing spatial distribution of dinoflagellate cyst assemblages in shal-low lagoons of southern New England (USA). Rev Palaeobot Palynol. 128(1–2):7–34.
Pospelova V, Esenkulova S, Johannessen SC, O’Brien MC, Macdonald RW. 2010. Organic-walled dinoflagellate cyst production, composition and flux from 1996 to 1998 in the central Strait of Georgia (BC, Canada): a sediment trap study. Mar Micropaleontol. 75(1–4):17–37.
Price AM, Pospelova V.2014. Spiniferites multisphaerus, a new dinoflagel-late cyst from the Late Quaternary of the Guaymas Basin, Gulf of California, Mexico. Palynology. 38(1):101–116.
Reid PC.1974. Gonyaulacacean dinoflagellate cysts from the British Isles. Nova Hedwigia. 25:579–637.
Rochon A, de Vernal A, Turon JL, Matthiessen J, Head MJ. 1999. Distribution of Dinoflagellate Cysts in Surface Sediments from the North Atlantic Ocean and Adjacent Basin and Quantitative Reconstruction of Sea-Surface Parameters. Dallas, TX: American Association of Stratigraphy Palynologists Foundation, AASP Contribution Series 35:146 pp.
Rossignol M.1964. Hystrichospheres du Quaternaire en Mediterranee ori-entale, dans les sediments pleistocenes et les boues marines actuelles. Rev Micropaleontol. 7:83–99.
Sarjeant WAS.1970. The genus Spiniferites Mantell, 1850 (Dinophyceae). Grana. 10(1):74–78.
Song Z, Guan X, Li Z, Zheng Y, Wang W, Hu Z. 1985. A research on Cenozoic palynology of the Longjing structural area in the Shelf Basin of the East China Sea (Donghai) region. China: Anhui Science and Technology Publishing House; p. 1–209. (Cenozoic-Mesozoic Palaeontology and Stratigraphy of East China, Series 1).
Sun X, Song Z. 1992. Quaternary dinoflagellates from arenaceous dolo-mite in Hainan Island. Acta Micropalaeontologica Sinica. 9:45–52. Suzuki A, Kurita H.1998. Finding of the Takinoue Molluscan fauna from
the Miocene Niniu Group at Fukuyama, Hobetsucho, Central Hokkaido. Jour Geol Soc Japan. 104(2):143–148.
Taylor FJR. 1980. On dinoflagellate evolution. BioSystems. 13(1–2):65–108.
Van Nieuwenhove N, Potvin E, Heikkil€a M, Pospelova V, Mertens KM, Masure E, Kucharska M, Yang EJ, Chomerat N, Zajaczkowski M.2018. Taxonomic revision of Spiniferites elongatus (the resting stage of Gonyaulax elongata) based on morphological and molecular analyses. Palynology. 42(S1). doi:10.1080/01916122.2018.1465736
Wall D, Dale B, Harada K.1973. Descriptions of new fossil dinoflagellates from the Late Quaternary of the Black Sea. Micropaleontology. 19(1):18–31.
Williams GL, Lentin JK, Fensome RA.1978. The Lentin and Williams index of fossil dinoflagellates, 1998 edition. Dallas, TX: American Association of Stratigraphic Palynologists Foundation, AASP Contribution Series. 34:817 pp.
Yun H. 1994. Emended stratigraphy of the Miocene formations in the Pohang Basin, Part II. South of the Hyongsan Fault. J Paleontol Soc Kor. 10:99–116.
Yun H, Yi S, Yi S, Kim JH, Byun HS, Kim GH, Park DB. 1999. Biostratigraphy and paleoenvironment of the Cheju Sedimentary Basin: Based on materials from exploration wells, Geobuk-1 and Okdom-1. J Paleontol Soc Kor. 15:43–94.
Yun H, Byun H, Park YA.2000. Paleoenvironments interpretation based on microfossil assemblages from intertidal sediments of the Haenam Bay. J Paleontol Soc Kor. 16:123–144.
Zhao Y, Morzadec-Kerfourn MT.1994. Nouveaux kystes de dinoflagelles: Spiniferites pacificus nov. sp. et Pentadinium netangei nov. sp. de Pleistocene du nord-ouest Pacifique. Geobios. 27(3):261–269. Zonneveld KAF, Marret F, Versteegh GJM, Bonnet S, Bouimetarhan I,
Crouch E, de Vernal A, Elshanawany R, Edwards L, Esper O, et al. 2013. Atlas of modern dinoflagellate cyst distribution based on 2405 datapoints. Rev Palaeobot Palynol. 191:1–197.
